Friday, March 4, 2016

What was the ancestor of flying Euparaves like?


Altogether the evidence is substantive that basal Euparaves* was a power-flying, primitive bird. It had extensive flying bird-like characteristics. And Oviraptors were secondarily flightless primitive birds.
The next question is: What was the ancestor of flying Euparaves like?
The first thing to notice is that the Euparaves flying bird-like characteristics appear at the base (origin) of Euparaves. They were not present in dinosaurs.
Consequently we will need to look at alternatives to the dinosaur to bird theory.

* "Euparaves" is the node based​ version of Paraves

1.0 Euparaves bird-like characteristics

Euparaves had extensive flying bird-like characteristics.

V-shaped furcula; advanced costosternal ventilator pump; initial arm flapping capability; further increased basal metabolic rate; cerebral expansion; increased egg size; iterative laying; increased laterally folding capability; monoautochronic ovulation; paternal care; partial pubis posterior orientation; slightly asymmetrical egg; short bony tail; three-fingered hand; symmetrical vaned feathers.
* NOTE: Only highly derived members (Pygostylia) had a short bony tail. Basal Euparaves had a long bony tail.
Arm elongation and thickening; initial aerial locomotion; extreme miniaturization; egg with increased asymmetry; improved contact incubation; partial knee-based locomotion; eggshell with low porosity; eggshell with third (external) layer; egg with unornamented surface; visually associated brain regions elaboration; asymmetrical vaned feathers.
* Note: Only derived members of Euparaves had asymmetrical vaned feathers. Basal Euparaves had symmetrical vaned feathers.

Basal paravians had many hallmark features necessary for flight, including extremely small body size; a laterally oriented, long, and robust forelimb; an enlarged forebrain and other derived neurological adaptations; and large flight feathers. 

(Xu et al 2014a)

2.0 Bird-like characteristics appeared at the base of Euparaves

The evidence indicates that the Euparaves flying bird-like characteristics appeared at the base of Euparaves.

Puttick et al were really surprised to discover that the key size shifts happened at the same time, at the origin of Paraves," (Puttick et al 2014).
Before the origin of Aves, on the branch leading to Paraves, high rates of evolution led to a smaller body size and a relatively larger forelimb in Paraves. These changes are on a single branch leading to Paraves, representing a shift to a new smaller size and larger forelimb at this point.
Paraves, rather than Aves alone, shifted to a different evolutionary model relative to other coelurosaurian theropods (Table 2). On all trees and for both femur and forelimb size, the model with a regime shift at Paraves, rather than Aves, is favored (Table S10). (Puttick et al 2014)

This suggests that large pennaceous feathers first evolved distally on the hindlimbs, as on the forelimbs and tail. This distal-first development led to a four-winged condition at the base of the Paraves. (Hu et al 2009)

The glenoid fossa faces ventrolaterally only shifted to a more lateral configuration at Paraves (Makovicky, Zanno 2011; Turner et al. 2012)

The significant lengthening and thickening of the forelimbs indicates a dramatic shift in forelimb function at the base of the Paraves, which might be related to the appearance of a degree of aerodynamic capability (Xu et al 2011)

Paraves, exclusive of Epidexipteryx hui, is marked by a suite of modifications to the shoulder girdle typically associated with the origin of the ‘‘avian’’ flight stroke (Ostrom, 1976b; Jenkins, 1993). The acromion margin of the scapula has a laterally everted anterior edge (char. 133.1) (fig. 55), the coracoid is inflected medially from the scapula forming an L-shaped scapulocoracoid in lateral view (char. 137.1) and the glenoid fossa faces laterally (char. 138.1) as opposed to the plesiomorphic posterior orientation (fig. 50). Additionally, the furcula is nearly symmetrical in shape as opposed to the asymmetry present in the furcula of more basal taxa (char. 474.1).
(Turner et al. 2012)

Larsson and Dececchi set out to determine from the fossil record when and how dinosaur forelimbs evolved into wings. Instead of finding a gradual lengthening, they found that when proportionate changes associated with different body sizes are factored out, there really is no such trend. The longer forelimbs, shorter hindlimbs, and long metatarsals (foot bones that are so long in birds they look like legs) appear abruptly in the fossil record. The skeletal characteristics of birds, in other words, start when birds start. They have no gradually transitioning antecedents in the rocks. 

“This decoupling may be fundamental to the success of birds, the most diverse class of land vertebrates on Earth today. The origin of birds and powered flight is a classic major evolutionary transition,” says Dececchi. “Our findings suggest that the limb lengths of birds had to be dissociated from general body size before they could radiate so successfully. It may be that this fact is what allowed them to become more than just another lineage of maniraptorans [dinosaurs presumed ancestral to birds] and led them to expand to the wide range of limb shapes and sizes present in today's birds.” He adds, “Knowing where birds came from, and how they got to where they are now, is crucial for understanding how the modern world came to look the way it is.” Referring to Dececchi and Larsson (2013):

Fossil evidence for changes in dinosaurs near the lineage leading to birds and the origin of flight has been sparse. A dinosaur from Mongolia represents the basal divergence within Dromaeosauridae. The taxon's small body size and phylogenetic position imply that extreme miniaturization was ancestral for Paraves, phylogenetically earlier than where flight evolution is strongly inferred. (Turner et al 2007)

The screamers are a small clade of birds (Anhimidae) The clade is exceptional within the living birds in lacking uncinate processes of ribs.[3] 

3.0 Claimed "stepwise" evolution of bird-like characteristics

A few researchers claim that the bird-like characteristics evolved "stepwise" from dinosaurs over a lengthy period of time. That is not correct. The characteristics appear at the base (origin) of Euparaves. These characteristics are not found in dinosaurs.
The iconic features of extant birds, for the most part, evolved in a gradual and stepwise fashion throughout theropod evolution. However, new data highlight occasional bursts of morphological novelty at certain stages close to the origin of birds and an unavoidable complex, mosaic evolutionary distribution of major bird characteristics on the theropod tree. ........ Newly discovered fossils and relevant analyses demonstrate that salient bird characteristics have a sequential and stepwise transformational pattern, with many arising early in dinosaur evolution, undergoing modifications through theropods, and finally approaching the modern condition close to the origin of the crown group birds (Fig. 2). For example, the unusually crouched hindlimb for bipedal locomotion that characterizes modern birds was acquired in stepwise fashion through much of theropod evolution (67), and both the furcula (68) and the “semilunate” carpal (69) appeared early in theropod evolution. Notably, major bird characteristics often exhibit a complex, mosaic evolutionary distribution throughout the theropod tree, and several evolutionary stages are characterized by accelerated changes (70). For example, the early evolution of paravian theropods features cerebral expansion and elaboration of visually associated brain regions (71), forelimb enlargement (22, 67), acquisition of a crouched, knee-based hindlimb locomotor system (67), and complex pinnate feathers associated with increased melanosome diversity, which implies a key physiological shift (72). Together these features may suggest the appearance of flight capability at the base of the Paraves (22, 67). (Xu et al 2014a)
Rather than a discrete transition from more-upright postures in the basal-most birds (Avialae) and their immediate outgroup deinonychosauria5,6, our results support hypotheses of a gradual, stepwise acquisition of more-crouched limb postures across much of theropod evolution1–4, although we find evidence of an accelerated change within the clade Maniraptora (birds and their closest relatives, such as deinonychosaurs). In addition, whereas reduction of the tail is widely accepted to be the primary morphological factor correlated with centre-of-mass position and, hence, evolution of hindlimb posture12345678, we instead find that enlargement of the pectoral limb and several associated trends have a much stronger influence. Intriguingly, our support for the onset of accelerated morpho-functional trends within Maniraptora is closely correlated with the evolution of flight. Because we find that the evolution of enlarged forelimbs is strongly linked, via whole-body centre of mass, to hindlimb function during terrestrial locomotion, we suggest that the evolution of avian flight is linked to anatomical novelties in the pelvic limb as well as the pectoral.
Visualization of the results indicates that this cranial shift was not evenly distributed or monotonic, but started sometime during the diversification of the clade Maniraptora (Fig. 3, between nodes 11 and 12) in the Jurassic period. (Allen et al (2013)

Homeotic transformation required 

The homology of the 'semilunate' carpal, an important structure linking non-avian and avian dinosaurs, has been controversial. Here we describe the morphology of some theropod wrists, demonstrating that the 'semilunate' carpal is not formed by the same carpal elements in all theropods possessing this feature and that the involvement of the lateralmost distal carpal in forming the 'semilunate' carpal of birds is an inheritance from their non-avian theropod ancestors. Optimization of relevant morphological features indicates that these features evolved in an incremental way and the 'semilunate' structure underwent a lateral shift in position during theropod evolution, possibly as a result of selection for foldable wings in birds and their close theropod relatives. We propose that homeotic transformation was involved in the evolution of the 'semilunate' carpal. In combination with developmental data on avian wing digits, this suggests that homeosis played a significant role in theropod hand evolution in general. (Xu, Han, Zhao 2014b)

The radiale angle progressively increased still further within Maniraptora, with concurrent elongation of the forelimb feathers and the forelimb itself. Carpal asymmetry would have permitted avian-like folding of the forelimb in order to protect the plumage, an early advantage of the flexible, asymmetric wrist inherited by birds [exaptation]. 
However, the measured value of 76° in Caudipteryx suggests that the oviraptorosaur wrist may have independently evolved an even greater abductor bias than that existing in avialans.
(Sullivan et al 2010)

4.0 Implausible Rates of Evolution Required

In order to explain the appearance out of the blue of the flying bird-like characteristics at the base of Paraves, dinosaur to bird theorists have worked out a story about how evolution itself worked at an implausible rate.

High rates were maintained only on the evolutionary line leading to birds, which continued to produce new ecological diversity not seen in other dinosaurs. Small body size might have been key to maintaining evolutionary potential (evolvability) in birds, which broke the lower body size limit of about 1 kg seen in other dinosaurs. Our results suggest that the maintenance of evolvability in only some lineages explains the unbalanced distribution of morphological and ecological diversity seen among groups of animals, both extinct and extant. Important living groups such as birds might therefore result from sustained, rapid evolutionary rates over timescales of hundreds of millions of years. (Benson et al 2014)

Before the origin of Aves, on the branch leading to Paraves, high rates of evolution led to a smaller body size and a relatively larger forelimb in Paraves. These changes are on a single branch leading to Paraves, representing a shift to a new smaller size and larger forelimb at this point. Rapid miniaturization and relative forelimb elongation at the root of Paraves explain the similarities between early birds and other Paraves (Padian and Chiappe 1998; Turner et al. 2007; Clarke and Middleton 2008; Novas et al. 2012). As with previous studies, we find strong evidence for paravian miniaturization (Xu et al. 2003; Turner et al. 2007; Novas et al. 2012) and no trend for forelimb elongation (Dececchi and Larrson 2013), but the identification here of increased rates of evolution of size-dependent forelimb and body size at the origin of Paraves emerges from our novel analytical approach. As with a recent study (Deccechi and Larrson 2013), we find evidence for a different allometric relationship between forelimb size and body size in Aves, but this result is altered by different phylogenetic topologies, and we find little evidence for elevated rates leading to or within Aves.(Puttick et al (2014)

Recent discoveries have highlighted the dramatic evolutionary transformation of massive, ground-dwelling theropod dinosaurs into light, volant birds. Here, we apply Bayesian approaches (originally developed for inferring geographic spread and rates of molecular evolution in viruses) in a different context: to infer size changes and rates of anatomical innovation (across up to 1549 skeletal characters) in fossils. These approaches identify two drivers underlying the dinosaur-bird transition. The theropod lineage directly ancestral to birds undergoes sustained miniaturization across 50 million years and at least 12 consecutive branches (internodes) and evolves skeletal adaptations four times faster than other dinosaurs. The distinct, prolonged phase of miniaturization along the bird stem would have facilitated the evolution of many novelties associated with small body size, such as reorientation of body mass, increased aerial ability, and paedomorphic skulls with reduced snouts but enlarged eyes and brains.
(Lee et al (2014)

The ancestors of Paraves first started to shrink in size in the early Jurassic 200 million years ago, and fossil evidence show that this theropod line evolved new adaptations four times faster than other groups of dinosaurs,[8] and was shrinking 160 times faster than other dinosaur lineages were growing.[9] 

Rates of morphological evolution can be quantified using time-calibrated phylogenetic trees. Brusatte et al. [1] employ the new phylogeny as the framework for conducting likelihood analyses of skeletal character evolution. These tests recover high rates of evolution both within the bird clade and also along a series of nodes on the theropod ‘backbone’ leading to birds. In agreement with these results, a recent Bayesian analysis using a different character dataset also found support for a sustained higher rate of skeletal evolution along this backbone [11], though the two studies disagree slightly on how deep in the tree the onset of higher rates occurs. A different set of tests in the Brusatte et al. [1] study compares rates between clades, revealing that birds as a clade exhibited a higher rate of skeletal evolution than other theropod clades. As a whole, these results suggest that birds are indeed a special case, leading to the hypothesis that the completion of the avian skeletal plan and development of powered flight opened the door to new ecological niches and triggered a burst of evolution [1]Here again, the lineage leading to birds stands out as an exception, with maniraptoran theropods sustaining high rates of size evolution relative to other dinosaur lineages[12]. A third recent study [13] employing likelihood methods capable of detecting branch-specific rate shifts places the shift to higher rates of size evolution on the branch leading to Paraves (Ksepka 2014)

5.0 Alternatives to the dinosaur to bird theory

There are two alternatives to the dinosaur to bird theory.

5.1 Basal archosaur hypothesis

One alternative is that there was a separate lineage from an unknown basal archosaur. This is called the basal archosaur hypothesis and has been documented by Alan Feduccia and a small band of others.
However there is reason to think this hypothesis may not be correct.

The origin of avian flight is a classic macroevolutionary transition with research spanning over a century. Two competing models explaining this locomotory transition have been discussed for decades: ground up versus trees down. Although it is impossible to directly test either of these theories, it is possible to test one of the requirements for the trees-down model, that of an arboreal paravian. We test for arboreality in non-avian theropods and early birds with comparisons to extant avian, mammalian, and reptilian scansors and climbers using a comprehensive set of morphological characters. Non-avian theropods, including the small, feathered deinonychosaurs, and Archaeopteryx, consistently and significantly cluster with fully terrestrial extant mammals and ground-based birds, such as ratites. Basal birds, more advanced than Archaeopteryx, cluster with extant perching ground-foraging birds. Evolutionary trends immediately prior to the origin of birds indicate skeletal adaptations opposite that expected for arboreal climbers. Results reject an arboreal capacity for the avian stem lineage, thus lending no support for the trees-down model. Support for a fully terrestrial ecology and origin of the avian flight stroke has broad implications for the origin of powered flight for this clade. A terrestrial origin for the avian flight stroke challenges the need for an intermediate gliding phase, presents the best resolved series of the evolution of vertebrate powered flight, and may differ fundamentally from the origin of bat and pterosaur flight, whose antecedents have been postulated to have been arboreal and gliding. (Dececchi, Larsson 2011)

5.2 Pterosaurs

To appreciate the other alternative we need to go back to the Ornithodira which is the common ancestor of dinosaurs and pterosaurs. Since birds did not evolve from dinosaurs, the other Ornithodiran possibility is pterosaurs.
This alternative was proposed by Seeley in the early 20th century but has not been pursued since.
This is a possible direction for further research.


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Jingmai O'Connor

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